Divergence In Reproductive Traits Research Articles

Character displacement of egg colors during tinamou speciation.

The divergence of reproductive traits frequently underpins the evolution of reproductive isolation. Here we investigated whether tinamou (Tinamidae) egg colorations function as mating signals that diverged as character displacement (mating signal character displacement hypothesis). We tested three evolutionary predictions behind the hypothesis: (a) egg colors coevolve with known mating signals; (b) signal divergence is associated with divergent habitat adaptation; and (c) sympatric tinamou species with similar songs have different egg colors as character displacement during speciation. We found support for all three predictions. In particular, egg colors coevolved with songs; songs and egg colors coevolved with habitat partitioning; and tinamou species that were likely sympatric with similar songs tended to have different egg colors. In conclusion, the mating signal character displacement hypothesis is well supported in which egg colors serve as mating signals that undergo character displacement during tinamou speciation.

Rapid colour shift by reproductive character displacement in Cupido butterflies.

Reproductive character displacement occurs when competition for successful breeding imposes a divergent selection on the interacting species, causing a divergence of reproductive traits. Here, we show that a disputed butterfly taxon is actually a case of male wing colour shift, apparently produced by reproductive character displacement. Using double digest restriction-site associated DNA sequencing and mitochondrial DNA sequencing we studied four butterfly taxa of the subgenus Cupido (Lepidoptera: Lycaenidae): Cupido minimus and the taxon carswelli, both characterized by brown males and females, plus C. lorquinii and C. osiris, both with blue males and brown females. Unexpectedly, taxa carswelli and C. lorquinii were close to indistinguishable based on our genomic and mitochondrial data, despite displaying strikingly different male coloration. In addition, we report and analysed a brown male within the C. lorquinii range, which demonstrates that the brown morph occurs at very low frequency in C. lorquinii. Such evidence strongly suggests that carswelli is conspecific with C. lorquinii and represents populations with a fixed male brown colour morph. Considering that these brown populations occur in sympatry with or very close to the blue C. osiris, and that the blue C. lorquinii populations never do, we propose that the taxon carswelli could have lost the blue colour due to reproductive character displacement with C. osiris. Since male colour is important for conspecific recognition during courtship, we hypothesize that the observed colour shift may eventually trigger incipient speciation between blue and brown populations. Male colour seems to be an evolutionarily labile character in the Polyommatinae, and the mechanism described here might be at work in the wide diversification of this subfamily of butterflies.

Sexual Selection and the Evolution of Male Reproductive Traits in Benthic Octopuses.

Competition between same-sex organisms, or intra-sexual selection, can occur before and after mating, and include processes such as sperm competition and cryptic female choice. One of the consequences of intra-sexual selection is that male reproductive traits tend to evolve and diverge at high rates. In benthic octopuses, females often mate with more than one male in a single reproductive event, opening the venue for intra-sexual selection at multiple levels. For instance, males transfer spermatophores through hectocotylus, and can remove the spermatophores left by other males. Considering the limited evidence on post-copula competition in benthic octopuses, and the potential to affect the evolution of reproductive traits within octopodids, we put this hypothesis to a test employing a phylogenetic comparative approach. We combined data on hectocotylized arm length (HAL), ligula length (LL), spermatophore length (SL) with a Bayesian molecular phylogeny of 87 species, to analyze how reproductive traits have diverged across lineages and covary with body size (mantle length; ML). First, additionally to ML, we estimated the phylogenetic signal (λ) and mode of evolution (κ) in each reproductive trait. Second, we performed phylogenetic regressions to quantify the association among reproductive traits and their co-variation with ML. This analysis allowed us to estimate the phenotypic change along a branch into the phylogeny, and whether selection may have played a role in the evolution and diversification of specific clades. Estimations of λ were always high (>0.75), indicating concordance between the traits and the topology of the phylogenetic tree. Low values of κ (<1.0) suggested that evolution depends on branch lengths. All reproductive traits exhibiting a positive relation with ML (β > 0.5 in all cases). Overall, evolutionary rate models applied to the SL-ML regression suggested that octopuses of the family Megaleledonidae have evolved larger spermatophores than expected for their size. The regression HAL-ML indicated that HAL was more variable in Megaleledonidae than in the remaining clades, suggesting that the high divergence across species within this group might partially reflect intra-sexual selection. These results support the hypothesis that, at least in some lineages, sexual selection may account for the divergence in reproductive traits of male octopuses.

Phylo-comparative analyses reveal the dual role of drift and selection in reproductive character displacement

When incipient species meet in secondary contact, natural selection can rapidly reduce costly reproductive interactions by directly targeting reproductive traits. This process, called reproductive character displacement (RCD), leaves a characteristic pattern of geographic variation where divergence of traits between species is greater in sympatry than allopatry. However, because other forces can also cause similar patterns, care must be given in separating pattern from process. Here we show how the phylo-comparative method together with genomic data can be used to evaluate evolutionary processes at the population level in closely related species. Using this framework, we test the role of RCD in speciation of two cricket species endemic to Anatolian mountains by quantifying patterns of character displacement, rates of evolution and adaptive divergence. Our results show differing patterns of character displacement between species for reproductive vs. non-reproductive characters and strong patterns of asymmetric divergence. We demonstrate diversification results from rapid divergence of reproductive traits towards multiple optima under the dual influence of strong drift and selection. These results present the first solid evidence for RCD in Anatolian mountains, quantify the amount of drift and selection necessary for RCD to lead to speciation, and demonstrate the utility of phylo-comparative methods for quantifying evolutionary parameters at the population level.

Low resource availability limits weed invasion of tropical savannas

The savanna biome is one of the least invaded among global biomes, although the mechanisms underpinning its resistance to alien species relative to other biomes is not well understood. Invaders generally are at the resource acquisitive end of functional global plant trait variation and in low-resource savanna environments we might expect that successful invaders will only outperform native species under resource rich or highly disturbed conditions. However, invaders may also directly exploit resource stressed environments using resource conservative traits in some situations. It’s also possible that successful invaders and native species largely overlap in their trait profiles indicating site specific environmental factors are responsible for invader success in particular contexts rather than a general trait and functional divergence between invaders and native species. To address these various hypotheses, we compared a suite of morphological and physiological traits in graminoid and herbaceous native and co-occurring invasive plant species across a range of habitats in savannas of the Kimberley region of northern Australia. Invader grass species had traits associated with resource acquisition and fast growth rates, such as high SLA and leaf nutrient contents. In contrast, dominant native perennial grasses had traits characteristic of resource conservation and slow growth in resource stressed conditions. Trait profiles among invasive forbs and legumes exhibited stress tolerant traits relative to their native counterparts. Invaders also displayed strong divergence in reproductive traits, suggesting diverse responses to disturbance not indicated by leaf economic traits alone. These results suggest that savannas may be resistant to invaders with resource acquisitive traits due to their strong resource limitation.

Reproductive character displacement and environmental filtering shape floral variation between sympatric sister taxa

Divergence in reproductive traits between closely related species that co-occur contributes to speciation by reducing interspecific gene flow. In flowering plants, greater floral divergence in sympatry than allopatry may reflect reproductive character displacement (RCD) by means of divergent pollinator-mediated selection or mating system evolution. However, environmental filtering (EF) would prevail for floral traits under stronger selection by abiotic factors than pollination, and lead to sympatric taxa being more phenotypically similar. We determine whether floral UV pigmentation and size show signatures of RCD or EF using a biogeographically informed sister taxa comparison. We determine whether 35 sister pairs in the Potentilleae tribe (Rosaceae) are allopatric or sympatric and confirm that sympatric sisters experience more similar bioclimatic conditions, an assumption of the EF hypothesis. We test whether interspecific differences are greater in allopatry or sympatry while accounting for divergence time. For UV pigmentation, sympatric sisters are more phenotypically similar than allopatric ones. For flower size, sympatric sisters show increased divergence with time since speciation but allopatric ones do not. We conclude that floral UV pigmentation shows a signature of EF, whereas flower size shows a signature of RCD. Discordant results between the traits suggest that the dominant selective agent differs between them.

Phenotypic divergence in reproductive traits of a moth population experiencing a phenological shift.

Allochrony that is reproductive isolation by time may further lead to divergence of reproductive adaptive traits in response to different environmental pressures over time. A unique “summer” population of the pine processionary moth Thaumetopoea pityocampa, reproductively isolated from the typical winter populations by allochronic differentiation, is here analyzed. This allochronically shifted population reproduces in the spring and develops in the summer, whereas “winter” populations reproduce in the late summer and have winter larval development. Both summer and winter populations coexist in the same pine stands, yet they face different climatic pressures as their active stages are present in different seasons. The occurrence of significant differences between the reproductive traits of the summer population and the typical winter populations (either sympatric or allopatric) is thus hypothesized. Female fecundity, egg size, egg covering, and egg parasitism were analyzed showing that the egg load was lower and that egg size was higher in the summer population than in all the studied winter populations. The scales that cover the egg batches of T. pityocampa differed significantly between populations in shape and color, resulting in a looser and darker covering in the summer population. The single specialist egg parasitoid species of this moth was almost missing in the summer population, and the overall parasitism rates were lower than in the winter population. Results suggest the occurrence of phenotypic differentiation between the summer population and the typical T. pityocampa winter populations for the life-history traits studied. This work provides an insight into how ecological divergence may follow the process of allochronic reproductive isolation.

Scent of a break-up: phylogeography and reproductive trait divergences in the red-tailed bumblebee (Bombus lapidarius)

BackgroundThe Pleistocene climatic oscillations are considered as a major driving force of intraspecific divergence and speciation. During Ice Ages, populations isolated in allopatric glacial refugia can experience differentiation in reproductive traits through divergence in selection regimes. This phenomenon may lead to reproductive isolation and dramatically accentuates the consequences of the climatic oscillations on species. Alternatively, when reproductive isolation is incomplete and populations are expanding again, further mating between the formerly isolated populations can result in the formation of a hybrid zone, genetic introgression or reinforcement speciation through reproductive trait displacements. Therefore changes in reproductive traits driven by population movements during climatic oscillations can act as an important force in promoting pre-zygotic isolation. Notwithstanding, divergence of reproductive traits has not been approached in the context of climatic oscillations. Here we investigate the impact of population movements driven by climatic oscillations on a reproductive trait of a bumblebee species (Bombus lapidarius). We characterise the pattern of variation and differentiation across the species distribution (i) with five genes (nuclear and mitochondrial), and (ii) in the chemical composition of male marking secretions (MMS), a key trait for mate attraction in bumblebees.ResultsOur results provide evidence that populations have experienced a genetic allopatric differentiation, in at least three main refugia (the Balkans, Centre-Eastern Europe, and Southern Italy) during Quaternary glaciations. The comparative chemical analyses show that populations from the Southern Italian refugium have experienced MMS differentiation and an incipient speciation process from another refugium. The meeting of Southern Italian populations with other populations as a result of range expansion at a secondary contact zone seems to have led to a reinforcement process on local MMS patterns.ConclusionsThis study suggests that population movement during Quaternary climatic oscillations can lead to divergence in reproductive traits by allopatric differentiation during Ice Ages and by reinforcement during post-glacial recolonization.

Plant community assembly in temperate forests along gradients of soil fertility and disturbance

Plant community assembly from a regional pool is largely driven by two mechanisms: environmental filtering and niche partitioning, which result in trait convergence or divergence, respectively. Although empirical evidence for both assembly mechanisms exists, the environmental conditions and traits where each of the two assembly patterns is prevalent remain unclear. We studied community assembly mechanisms in herb layer communities of temperate forest patches in NW Germany, looking at distributions of competitive and reproductive traits along gradients of soil fertility and disturbance. We also examined how community assembly patterns changed over a time span of two decades. Canopy height converged toward taller species with increasing soil fertility and increasing light availability. Most reproductive traits diverged with an increasing degree of disturbance and with increasing fertility. Comparisons over time indicated that disturbance events induced the coexistence of species with different reproductive strategies and also selected for tall species as a result of enhanced competitive pressure. Our study demonstrates that in accordance with existing hypotheses, competitive traits (e.g., canopy height) can be convergent in favorable environments. However, this convergence is associated with a divergence of traits related to other challenges (e.g., reproduction), indicating that true functional redundancy within communities does not exist. Moreover, our study shows that the expected divergence of reproductive traits at disturbed sites can be accompanied by a convergence of other traits (e.g., canopy height), indicating that several assembly mechanisms can operate simultaneously.

Generational shape shifting: changes in egg shape and size between sexual and asexual generations of a cyclically parthenogenic gall former

Successive generations of multivoltine species experience selection specific to the spatiotemporal environments encountered that may lead to adaptive divergence in reproductive traits among generations. To compare reproductive effort within and between generations, appropriate volumetric models, selected on the basis of the analysis of egg shape, are required to estimate the sizes (volumes) of individual eggs. We assessed the shape and estimated the volume of individual eggs produced by the temporally and spatially segregated sexual and asexual generations of the gall former, Belonocnema treatae Mayr (Hymenoptera: Cynipini: Cynipidae). Egg shape, indexed as the difference between the polar and equatorial axes of the ellipsoidal eggs, was independent of egg size, but differed between generations. The relationship of egg shape and female body size within and between generations confirmed that egg shape is an intrinsic property of each generation. Generational differences in egg shape then informed the selection of volumetric models to estimate egg size. We modeled asexual generation eggs as both spheres and prolate spheroids, and sexual generation eggs as both cylinders and prolate spheroids. Choice of volumetric model changed estimates of egg size within the asexual generation by 23% and within the sexual generation by 50%. Comparisons between generations based on the above models produced estimated differences in egg volume that ranged from 16 to 114%. In both generations, a prolate spheroid was the most parsimonious model of egg volume. Based on this model, sexual generation eggs averaged 43% larger than asexual generation eggs. The increased size of sexual eggs was achieved via conservation of the egg’s equatorial axis and elongation of the polar axis. The shift in egg shape between sexual and asexualB.treatae is the first documented dimorphism in an egg characteristic expressed between generations of a cyclically parthenogenic organism.

INCREASED FLORAL DIVERGENCE IN SYMPATRIC MONKEYFLOWERS

Sympatric sister species are predicted to have greater divergence in reproductive traits than allopatric sister species, especially if mating system shifts, such as the evolution of self-fertilization, are more likely to originate within the geographic range of the outcrossing ancestor. We present evidence that supports this expectation-sympatric sister species in the monkeyflower genus, Mimulus, exhibit greater divergence in flower size than allopatric sister species. Additionally, we find that sympatric sister species are more likely to have one species with anthers that overtop their stigmas than allopatric sister species, suggesting that the evolution of automatic self-pollination may contribute to this pattern. Potential mechanisms underlying this pattern include reinforcement and a stepping stone model of parapatric speciation.

Courtship and mating behaviour of the brilliant-thighed frog Allobates femoralis from Central Amazonia: implications for the study of a species complex

The identification of divergence in reproductive traits may substantially improve integrative approaches to understand species limits within clades that are suspected to contain cryptic diversity. The frog Allobates femoralis has been regarded as a pan-Amazonian species, and widely used as a model for addressing evolutionary issues regarding patterns of intraspecific diversification, social organisation, and animal communication. Recent accumulation of genetic, morphological, and bioacoustic data gathered from different localities strongly supports the idea that it represents a species complex, but field behavioural observations related to courtship and mating are surprisingly scarce. Here, we provide a description of several aspects of the reproductive biology of A. femoralis from a Central Amazon site, and compare our results with the few published reports for the species. This study demonstrated that, besides the known divergence in the number of notes of the A. femoralis call, there are both quantitative and qualitative differences regarding reproductive traits between two populations of this taxon. The most striking difference was the observation of cephalic amplexus in the population from the Reserva Ducke, Brazil, which contrasts with the absence of any kind of body contact between A. femoralis pairs during mating interactions at the Panguana Biological Station, Peru. In addition, we report for the first time a set of visual components of the courtship behaviour, such as throat display, limb lifting, circling, and leg stretching. Behavioural differences can lead to a pre-zygotic isolation, thus representing a first step in the speciation process through differential sexual preferences. Hence, our finding of divergence in a set of traits probably related to mate recognition and choice is surprising within populations assigned to a single clade, and highlights the importance of considering behavioural traits in order to disentangle the evolutionary forces driving the diversification of A. femoralis.

REPRODUCTIVE CHARACTER DISPLACEMENT AND SIGNAL ONTOGENY IN A SYMPATRIC ASSEMBLAGE OF ELECTRIC FISH

The reproductive signals of two or more taxa may diverge in areas of sympatry, due to selection against costly reproductive interference. This divergence, termed reproductive character displacement (RCD), is expected in species-rich assemblages, where interspecific signal partitioning among closely related species is common. However, RCD is usually documented from simple two-taxon cases, via geographical tests for greater divergence of reproductive traits in sympatry than in allopatry. We propose a novel approach to recognizing and understanding RCD in multi-species communities--one that traces the displacement of signals within multivariate signal space during the ontogeny of individual animals. We argue that a case for RCD can be made if the amount of signal displacement between a pair of species after maturation is negatively correlated to distance in signal space before maturation. Our application of this approach, using a dataset of communication signals from a sympatric Amazonian assemblage of the electric fish genus Gymnotus, provides strong evidence for RCD among multiple species. We argue that RCD arose from the costs of heterospecific mismating, but interacted with sexual selection--favoring the evolution of conspicuous male signals that not only serve for mate-choice, but which simultaneously facilitate species recognition.

Natural selection hampers divergence of reproductive traits in a seed beetle

Speciation is thought to often result from indirect selection for reproductive isolation. This will occur when reproductive traits that cause reproductive isolation evolve (i) as a by-product of natural selection on traits with which they are genetically correlated or (ii) as an indirect result of diversifying sexual selection. Here, we use experimental evolution to study the degree of divergent evolution of reproductive traits by manipulating the intensity of natural and sexual selection in replicated selection lines of seed beetles. Following 40 generations of selection, we assayed the degree of divergent evolution of reproductive traits between replicate selection lines experiencing the same selection regime. The evolution of reproductive traits was significantly divergent across selection lines within treatments. The evolution of reproductive traits was both slower and, more importantly, significantly less divergent among lines experiencing stronger directional natural selection. This suggests that reproductive traits did not evolve as an indirect by-product of adaptation. We discuss several ways in which natural selection may hamper divergent evolution among allopatric populations.